Structural basis of p75 transmembrane domain dimerization

Journal of Biological Chemistry

Volumn 291, Issue 23, 2016, Pages 12346-12357

  Nadezhdin, Kirill D ^a   García Carpio, Irmina ^b   Goncharuk, Sergey A ^a   Mineev, Konstantin S ^a   Arseniev, Alexander S ^a   Vilar, Marçal ^b,c  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; CHEMICAL ACTIVATION; CONFORMATIONS; COVALENT BONDS; DIMERIZATION;

ACTIVATION MECHANISMS; INTRAMEMBRANE PROTEOLYSIS; MONOMER-DIMER EQUILIBRIUM; P75 NEUROTROPHIN RECEPTOR; THREE-DIMENSIONAL STRUCTURE; TRANS-MEMBRANE DOMAINS; TRANSMEMBRANE DOMAIN; TRANSMEMBRANE RECEPTORS;

DIMERS;

CYSTEINE; DIMER; NERVE GROWTH FACTOR; PROTEIN P75; LIPID; MEMBRANE PROTEIN; MICELLE; NERVE GROWTH FACTOR RECEPTOR;

ALPHA HELIX; ARTICLE; CONTROLLED STUDY; DIMERIZATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STABILITY; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MICELLE; MOLECULAR MODEL; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION REDUCTION REACTION; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; WESTERN BLOTTING;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BLOTTING, WESTERN; CYSTEINE; HELA CELLS; HUMANS; LIPIDS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS; MICELLES; MODELS, MOLECULAR; MUTATION; OXIDATION-REDUCTION; PROTEIN DOMAINS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEOLYSIS; RECEPTOR, NERVE GROWTH FACTOR;

EID: 84974621145     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.723585     Document Type: Article

References (69)

1. Friedman, W. J., and Greene, L. A. (1999) Neurotrophin signaling via Trks and p75. Exp. Cell Res. 253, 131-142
2. Liepinsh, E., Ilag, L. L., Otting, G., and Ibáñez, C. F. (1997) NMR structure of the death domain of the p75 neurotrophin receptor. EMBO J. 16, 4999-5005
3. Ibáñez, C. F., and Simi, A. (2012) p75 neurotrophin receptor signaling in nervous system injury and degeneration: paradox and opportunity. Trends Neurosci. 35, 431- 440
4. Yamashita, T., Fujitani, M., Hata, K., Mimura, F., and Yamagishi, S. (2005) Diverse functions of the p75 neurotrophin receptor. Anat. Sci. Int. 80, 37-41
5. Nykjaer, A., Willnow, T. E., and Petersen, C. M. (2005) p75NTR-live or let die. Curr. Opin. Neurobiol. 15, 49-57
6. Roux, P. P., and Barker, P. A. (2002) Neurotrophin signaling through the p75 neurotrophin receptor. Prog. Neurobiol. 67, 203-233
7. Vilar, M., Charalampopoulos, I., Kenchappa, R. S., Reversi, A., Klos-Applequist, J. M., Karaca, E., Simi, A., Spuch, C., Choi, S., Friedman, W. J., Ericson, J., Schiavo, G., Carter, B. D., and Ibáñez, C. F. (2009) Ligand-independent signaling by disulfide-crosslinked dimers of the p75 neurotrophin receptor. J. Cell Sci. 122, 3351-3357
8. Vilar, M., Charalampopoulos, I., Kenchappa, R. S., Simi, A., Karaca, E., Reversi, A., Choi, S., Bothwell, M., Mingarro, I., Friedman, W. J., Schiavo, G., Bastiaens, P. I., Verveer, P. J., Carter, B. D., and Ibáñez, C. F. (2009) Activation of the p75 neurotrophin receptor through conformational rearrangement of disulphide-linked receptor dimers. Neuron 62, 72-83
9. Sykes, A. M., Palstra, N., Abankwa, D., Hill, J. M., Skeldal, S., Matusica, D., Venkatraman, P., Hancock, J. F., and Coulson, E. J. (2012) The effects of transmembrane sequence and dimerization on cleavage of the p75 neurotrophin receptor by gamma-secretase. J. Biol. Chem. 287, 43810-43824
10. Anastasia, A., Barker, P. A., Chao, M. V., and Hempstead, B. L. (2015) Detection of p75NTR trimers: implications for receptor stoichiometry and activation. J. Neurosci. 35, 11911-11920
11. Wiesmann, C., and de Vos, A. M. (2001) Nerve growth factor: structure and function. Cell. Mol. Life Sci. 58, 748-759
12. Grob, P. M., Berlot, C. H., and Bothwell, M. A. (1983) Affinity labeling and partial purification of nerve growth factor receptors from rat pheochro-mocytoma and human melanoma cells. Proc. Natl. Acad. Sci. U.S.A. 80, 6819-6823
13. Gong, Y., Cao, P., Yu, H. J., and Jiang, T. (2008) Crystal structure of the neurotrophin-3 and p75NTR symmetrical complex. Nature 454, 789-793
14. Feng, D., Kim, T., Ozkan, E., Light, M., Torkin, R., Teng, K. K., Hempstead, B. L., and Garcia, K. C. (2010) Molecular and structural insight into proNGF engagement of p75NTR and sortilin. J. Mol. Biol. 396, 967-984
15. Aurikko, J. P., Ruotolo, B. T., Grossmann, J. G., Moncrieffe, M. C., Stephens, E., Leppänen, V. M., Robinson, C. V., Saarma, M., Bradshaw, R. A., and Blundell, T. L. (2005) Characterization of symmetric complexes of nerve growth factor and the ectodomain of the pan-neurotrophin receptor, p75NTR. J. Biol. Chem. 280, 33453-33460
16. He, X. L., and Garcia, K. C. (2004) Structure of nerve growth factor complexed with the shared neurotrophin receptor p75. Science 304, 870- 875
17. Vilar, M., Sung, T. C., Chen, Z., García-Carpio, I., Fernandez, E. M., Xu, J., Riek, R., and Lee, K. F. (2014) Heterodimerization of p45-p75 modulates p75 signaling: structural basis and mechanism of action. PLos Biol. 12, e1001918
18. Lin, Z., Tann, J. Y., Goh, E. T., Kelly, C., Lim, K. B., Gao, J. F., and Ibanez, C. F. (2015) Structural basis of death domain signaling in the p75 neurotrophin receptor. eLife 4, e11692
19. Wehrman, T., He, X., Raab, B., Dukipatti, A., Blau, H., and Garcia, K. C. (2007) Structural and mechanistic insights into nerve growth factor interactions with the TrkA and p75 receptors. Neuron 53, 25-38
20. Jiang, G., and Hunter, T. (1999) Receptor signaling: when dimerization is not enough. Curr. Biol. 9, R568-R571
21. Mineev, K. S., Goncharuk, S. A., Kuzmichev, P. K., Vilar, M., and Arseniev, A. S. (2015) NMR dynamics of transmembrane and intracellular domains of p75NTR in lipid-protein nanodiscs. Biophys. J. 109, 772-782
22. Aoki, M., Matsuda, T., Tomo, Y., Miyata, Y., Inoue, M., Kigawa, T., and Yokoyama, S. (2009) Automated system for high-throughput protein production using the dialysis cell-free method. Protein Expr. Purif. 68, 128-136
23. Kai, L., Roos, C., Haberstock, S., Proverbio, D., Ma, Y., Junge, F., Karbyshev, M., Dötsch, V., and Bernhard, F. (2012) Systems for the cell-free synthesis of proteins. Methods Mol. Biol. 800, 201-225
24. Schwarz, D., Junge, F., Durst, F., Frölich, N., Schneider, B., Reckel, S., Sobhanifar, S., Dötsch, V., and Bernhard, F. (2007) Preparative scale expression of membrane proteins in Escherichia coli-based continuous exchange cell-free systems. Nat. Protoc. 2, 2945-2957
25. Schägger, H., and von Jagow, G. (1987) Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379
26. Goncharuk, S. A., Goncharuk, M. V., Mayzel, M. L., Lesovoy, D. M., Chupin, V. V., Bocharov, E. V., Arseniev, A. S., and Kirpichnikov, M. P. (2011) Bacterial synthesis and purification of normal and mutant forms of human FGFR3 transmembrane segment. Acta Naturae 3, 77- 84
27. Keller, R. L. J. (2004) The Computer Aided Resonance Assignment Tutorial, CANTINA Verlag, Goldau, Switzerland
28. Cavanagh, J., Fairbrother, W. J., Palmer, A. G., and Skelton, N. J. (2006) Protein NMR Spectroscopy: Principles and Practice, 2nd Ed., Academic Press, San Diego, CA
29. Güntert, P. (2004) Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278, 353-378
30. Shen, Y., and Bax, A. (2013) Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks. J. Biomol. NMR 56, 227-241
31. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55, 29-32
32. Polyansky, A. A., Chugunov, A. O., Volynsky, P. E., Krylov, N. A., Nolde, D. E., and Efremov, R. G. (2014) PREDDIMER: a web server for prediction of transmembrane helical dimers. Bioinformatics 30, 889-890
33. Berger, B. W., Kulp, D. W., Span, L. M., DeGrado, J. L., Billings, P. C., Senes, A., Bennett, J. S., and DeGrado, W. F. (2010) Consensus motif for integrin transmembrane helix association. Proc. Natl. Acad. Sci. U.S.A. 107, 703-708
34. Kanning, K. C., Hudson, M., Amieux, P. S., Wiley, J. C., Bothwell, M., and Schecterson, L. C. (2003) Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-terminal fragments with signaling capability. J. Neurosci. 23, 5425-5436
35. Mineev, K. S., Lesovoy, D. M., Usmanova, D. R., Goncharuk, S. A., Shulepko, M. A., Lyukmanova, E. N., Kirpichnikov, M. P., Bocharov, E. V., and Arseniev, A. S. (2014) NMR-based approach to measure the free energy of transmembrane helix-helix interactions. Biochim. Biophys. Acta 1838, 164-172
36. Chen, L., Novicky, L., Merzlyakov, M., Hristov, T., and Hristova, K. (2010) Measuring the energetics of membrane protein dimerization in mammalian membranes. J. Am. Chem. Soc. 132, 3628-3635
37. Fisher, L. E., Engelman, D. M., and Sturgis, J. N. (2003) Effect of detergents on the association of the glycophorin a transmembrane helix. Biophys. J. 85, 3097-3105
38. Fleming, K. G. (2002) Standardizing the free energy change of transmembrane helix-helix interactions. J. Mol. Biol. 323, 563-571
39. Bocharov, E. V., Mineev, K. S., Goncharuk, M. V., and Arseniev, A. S. (2012) Structural and thermodynamic insight into the process of "weak" dimerization of the ErbB4 transmembrane domain by solution NMR. Biochim. Biophys. Acta 1818, 2158-2170
40. Bocharov, E. V., Lesovoy, D. M., Goncharuk, S. A., Goncharuk, M. V., Hristova, K., and Arseniev, A. S. (2013) Structure of FGFR3 transmembrane domain dimer: implications for signaling and human pathologies. Structure 21, 2087-2093
41. Russ, W. P., and Engelman, D. M. (2000) The GxxxG motif: a framework for transmembrane helix-helix association. J. Mol. Biol. 296, 911-919
42. Fink, A., Sal-Man, N., Gerber, D., and Shai, Y. (2012) Transmembrane domains interactions within the membrane milieu: principles, advances and challenges. Biochim. Biophys. Acta 1818, 974-983
43. Walters, R. F., and DeGrado, W. F. (2006) Helix-packing motifs in membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 103, 13658-13663
44. Polyansky, A. A., Volynsky, P. E., and Efremov, R. G. (2012) Multistate organization of transmembrane helical protein dimers governed by the host membrane. J. Am. Chem. Soc. 134, 14390-14400
45. Russ, W. P., and Engelman, D. M. (1999) TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc. Natl. Acad. Sci. U.S.A. 96, 863-868
46. Teese, M. G., and Langosch, D. (2015) Role of GxxxG motifs in transmembrane domain interactions. Biochemistry 54, 5125-5135
47. Kenchappa, R. S., Tep, C., Korade, Z., Urra, S., Bronfman, F. C., Yoon, S. O., and Carter, B. D. (2010) p75 neurotrophin receptor-mediated apoptosis in sympathetic neurons involves a biphasic activation of JNK and up-regulation of tumor necrosis factor-α-converting enzyme/ADAM17. J. Biol. Chem. 285, 20358-20368
48. Kenchappa, R. S., Zampieri, N., Chao, M. V., Barker, P. A., Teng, H. K., Hempstead, B. L., and Carter, B. D. (2006) Ligand-dependent cleavage of the p75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron 50, 219-232
49. Vicario, A., Kisiswa, L., Tann, J. Y., Kelly, C. E., and Ibáñez, C. F. (2015) Neuron-type-specific signaling by the p75NTR death receptor regulated by differential proteolytic cleavage. J. Cell Sci. 128, 1507-1517
50. Skeldal, S., Matusica, D., Nykjaer, A., and Coulson, E. J. (2011) Proteolytic processing of the p75 neurotrophin receptor: a prerequisite for signalling?: neuronal life, growth and death signalling are crucially regulated by intramembrane proteolysis and trafficking of p75(NTR). BioEssays 33, 614- 625
51. Nakano, M., Fukuda, M., Kudo, T., Miyazaki, M., Wada, Y., Matsuzaki, N., Endo, H., and Handa, T. (2009) Static and dynamic properties of phospholipid bilayer nanodiscs. J. Am. Chem. Soc. 131, 8308-8312
52. Mineev, K. S., Bocharov, E. V., Volynsky, P. E., Goncharuk, M. V., Tkach, E. N., Ermolyuk, Y. S., Schulga, A. A., Chupin, V. V., Maslennikov, I. V., Efremov, R. G., and Arseniev, A. S. (2011) Dimeric structure of the transmembrane domain of glycophorin a in lipidic and detergent environments. Acta Naturae 3, 90-98
53. Bocharov, E. V., Pustovalova, Y. E., Pavlov, K. V., Volynsky, P. E., Goncharuk, M. V., Ermolyuk, Y. S., Karpunin, D. V., Schulga, A. A., Kirpichnikov, M. P., Efremov, R. G., Maslennikov, I. V., and Arseniev, A. S. (2007) Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger. J. Biol. Chem. 282, 16256-16266
54. Sulistijo, E. S., and Mackenzie, K. R. (2009) Structural basis for dimerization of the BNIP3 transmembrane domain. Biochemistry 48, 5106-5120
55. Smith, S. O., Song, D., Shekar, S., Groesbeek, M., Ziliox, M., and Aimoto, S. (2001) Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers. Biochemistry 40, 6553-6558
56. Mineev, K. S., Panova, S. V., Bocharova, O. V., Bocharov, E. V., and Arseniev, A. S. (2015) The membrane mimetic affects the spatial structure and mobility of EGFR transmembrane and juxtamembrane domains. Biochemistry 54, 6295-6298
57. MacKenzie, K. R., Prestegard, J. H., and Engelman, D. M. (1997) A transmembrane helix dimer: structure and implications. Science 276, 131-133
58. Zhou, P., Tian, F., Lv, F., and Shang, Z. (2009) Geometric characteristics of hydrogen bonds involving sulfur atoms in proteins. Proteins 76, 151-163
59. Mao, G., Tan, J., Cui, M. Z., Chui, D., and Xu, X. (2009) The GxxxG motif in the transmembrane domain of AβPP plays an essential role in the interaction of CTFβ with the γ-secretase complex and the formation of amyloid-oβ. J. Alzheimers Dis. 18, 167-176
60. Jung, K. M., Tan, S., Landman, N., Petrova, K., Murray, S., Lewis, R., Kim, P. K., Kim, D. S., Ryu, S. H., Chao, M. V., and Kim, T. W. (2003) Regulated intramembrane proteolysis of the p75 neurotrophin receptor modulates its association with the TrkA receptor. J. Biol. Chem. 278, 42161-42169
61. Bhakar, A. L., Howell, J. L., Paul, C. E., Salehi, A. H., Becker, E. B., Said, F., Bonni, A., and Barker, P. A. (2003) Apoptosis induced by p75NTR overexpression requires Jun kinase-dependent phosphorylation of Bad. J. Neurosci. 23, 11373-11381
62. Wang, K. C., Kim, J. A., Sivasankaran, R., Segal, R., and He, Z. (2002) p75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420, 74-78
63. Nykjaer, A., Lee, R., Teng, K. K., Jansen, P., Madsen, P., Nielsen, M. S., Jacobsen, C., Kliemannel, M., Schwarz, E., Willnow, T. E., Hempstead, B. L., and Petersen, C. M. (2004) Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843-848
64. Hempstead, B. L., Martin-Zanca, D., Kaplan, D. R., Parada, L. F., and Chao, M. V. (1991) High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 350, 678-683
65. Rath, A., Glibowicka, M., Nadeau, V. G., Chen, G., and Deber, C. M. (2009) Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 106, 1760-1765
66. Yamashita, T., Higuchi, H., and Tohyama, M. (2002) The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J. Cell Biol. 157, 565-570
67. Fu, Q., Fu, T. M., Cruz, A. C., Sengupta, P., Thomas, S. K., Wang, S., Siegel, R. M., Wu, H., and Chou, J. J. (2016) Structural basis and functional role of intramembrane trimerization of the Fas/CD95 death receptor. Mol. Cell 61, 602-613
68. Johnson, D., Lanahan, A., Buck, C. R., Sehgal, A., Morgan, C., Mercer, E., Bothwell, M., and Chao, M. (1986) Expression and structure of the human NGF receptor. Cell 47, 545-554
69. Bothwell, M. (2006) Evolution of the neurotrophin signaling system in invertebrates. Brain Behav. Evol. 68, 124-132